Gut microbes influence fitness and malaria transmission potential of Asian malaria vector Anopheles stephensi

Acta Tropica

Volumn 128, Issue 1, 2013, Pages 41-47

  Sharma, Anil ^a   Dhayal, Devender ^b   Singh, O P ^b   Adak, T ^b   Bhatnagar, Raj K ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY ICGEB   (India)

^b NATIONAL INSTITUTE OF MALARIA RESEARCH   (India)

Author keywords

Anopheles; Fecundity; Gut biota; Longevity; Malaria transmittance

Indexed keywords

DISEASE TRANSMISSION; DISEASE VECTOR; FECUNDITY; FITNESS; HOST-PARASITE INTERACTION; LONGEVITY; MALARIA; MICROBIAL COMMUNITY; MOSQUITO;

ANOPHELES STEPHENSI; ARTICLE; DIGESTION; DISEASE PREDISPOSITION; ECOLOGICAL NICHE; EGG LAYING; FEMALE; INSTRUMENT STERILIZATION; INTESTINE FLORA; LONGEVITY; MALARIA; MALARIA CONTROL; MALE; MICROBIAL COMMUNITY; MICROORGANISM; MIDGUT; NONHUMAN; OOCYST; OOCYTE DEVELOPMENT; OVARY; PARASITE DEVELOPMENT; PARASITE TRANSMISSION; PLASMODIUM;

ANOPHELES STEPHENSI;

ANOPHELES; FECUNDITY; GUT-BIOTA; LONGEVITY; MALARIA TRANSMITTANCE;

ANIMALS; ANOPHELES; ASIA; BIOTA; FEEDING BEHAVIOR; FEMALE; FERTILITY; GASTROINTESTINAL TRACT; LONGEVITY; MALARIA; MALE; PLASMODIUM;

EID: 84883742033     PISSN: 0001706X     EISSN: 18736254     Source Type: Journal    
DOI: 10.1016/j.actatropica.2013.06.008     Document Type: Article

References (59)

1. Adak T., Kaur S., Singh O.P. Comparative susceptibility of different members of the Anopheles culicifacies complex to Plasmodium vivax. Trans. R. Soc. Trop. Med. Hyg. 1999, 93:573-577.
2. Barret E.L.B., Prezios R.F., Moore A.J., Moore P.J. Effects of mating delay and nutritional signals on resource cycling in a cyclically breeding cockroach. J. Insect Physiol. 2008, 54:25-31.
3. Bilker O., Shaw M.K., Margos G., Sinden R.E. The roles of temperature, pH and mosquito factors as triggers of male and female gametogenesis of Plasmodium berghei in vitro. Parasitology 1997, 115:1-7.
4. Bourtzis K., Miller T. Insect Symbiosis 2003, 347. CRC Press, Boca Raton.
5. Briegel H. Determination of uric acid and hematin in a single sample of excreta from blood fed insects. Experientia 1980, 36:1428.
6. Brodersen D.E., Clemons W.M., Carter A.P., Morgan-Warren R.J., Wimberly B.T., Ramakrishnan V. The structural basis for the action of the antibiotics tetracycline, pactamycin, and hygromycin B on the 30S ribosomal subunit. Cell 2000, 103:1143-1154.
7. Bruce-Chwatt L.J. Ronald Ross, William Gorgas and malaria eradication. Am. J. Trop. Med. Hyg. 1977, 26:1071-1079.
8. Brummel T., Ching A., Seroude L., Simon A.F., Benzer S. Drosophila lifespan enhancement by exogenous bacteria. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:12974-12979.
9. Buchon N., Broderick N.A., Chackrabrati S., Lemaitre B. Invasive and indigeneous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev. 2009, 23:2333-2344.
10. Buchon N., Broderick N.A., Poidevin M., Pradervand S., Lemaitre B. Drosophila intestinal response to bacterial infection: activation of host defence and stem cell proliferation. Cell Host Microbe 2009, 5:200-211.
11. Canudas-Romo V. Three measures of longevity: time trends and record values. Demography 2010, 4:299-312.
12. Chavshin A.R., Oshaghi M.A., Vatandoost H., Pourmand M.R., Raeisi A., Enayati A.A., Mardani N., Ghoorchian S. Identification of bacterial microflora in the midgut of the larvae and adult of wild caught Anopheles stephensi: A step toward finding suitable paratransgenesis candidates. Acta Trop. 2012, 121:129-134.
13. Cirimotich C.M., Dong Y., Clayton A.M., Sandiford S.L., Souza-Neto J.A., Mulenga M., Dimopoulos G. Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science 2011, 332:855-858.
14. Clements A.N., Bocock M.R. Ovarian development in mosquitoes: stages of growth and arrest, and follicular resorption. Physiol. Entomol. 1984, 9:1-8.
15. Croll N.A., Smith J.M., Zuckerman B.M. The aging process of the nematode Caenorhabditis elegans in bacterial and axenic culture. Exp. Aging Res. 1977, 3:175-189.
16. Cronin S.J., Nehme N.T., Limmer S., Liegeosis S., Pospisilik J.A., Schramek D., Leibbrandt A., Simoes Rde M., Gruber S., Puc U., Ebersberger I., Zoranovic T., Neely G.G., von Haeseler A., Ferrandon D., Penninger J.M. Genome-wide RNAi screen identifies genes involved in intestinal pathogenic bacterial infection. Science 2009, 325:340-343.
17. Dash A.P., Adak T., Raghavendra K., Singh O.P. The biology and control of malaria vectors in India. Curr. Sci. 2007, 92:1571-1578.
18. Dillon R.J., Dillon V.M. The gut bacteria of insects: nonpathogenic interactions. Annu. Rev. Entomol. 2004, 49:71-92.
19. Dobson S.L., Marsland E.J., Rattanadechakul W. Mutualistic Wolbachia infection in Aedes albopictus accelerating cytoplasmic drive. Genetics 2002, 160:1087-1094.
20. Dong Y., Manfredini F., Dimopoulos G. Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog. 2009, 5:e1000423.
21. Favia G., Ricci I., Scuppa P., Damiani C., Rossi P., Capone A., Freece C.D., Valzano M., Cappelli A., Mosca M., Ulissi U. Facing malaria parasite with mosquito symbionts. Malaria Parasites 2012, 57-70. InTechOpen. O. Omolade, Okwa (Eds.).
22. Fouda M.A., Hassan M.I., Al-Daly A.G., Hammad K.M. Effect of midgut bacteria of Culex pipiens L. on digestion and reproduction. J. Egypt Soc. Parasitol. 2001, 31:767-780.
23. Gad A.M., Maier W.A., Piekarski G. Pathology of Anopheles stephensi after infection with Plasmodium berghei berghei. Z. Parasitenkd. 1979, 60:249-261.
24. Garigan D., Hsu A.L., Fraser A.G., Kamath R.S., Ahringer J., Kenyon C. Genetic analysis of tissue aging in Caenorhabditis elegans: a role for heat-shock factor and bacterial proliferation. Genetics 2002, 161:1101-1112.
25. Gonzalez-Ceron L., Santillan F., Rodriguez M.H., Mendez D., Hernandez-Avila J.E. Bacteria in midguts of field-collected Anopheles albimanus block Plasmodium vivax sporogonic development. J. Med. Entomol. 2003, 40:371-374.
26. Hattori M., Taylor T.D. The human intestinal microbiome: a new frontier of human biology. DNA Res. 2009, 16:1-12.
27. Hoc T.Q. Ovulation and post-ovulation changes in the terminal region of the ovarioles of the mosquito Aedes aegypti (L.) (Diptera: Culicidae). Ann. Trop. Med. Parasitol. 1996, 90:71-78.
28. Houthoofd K., Braeckman B.P., Lenaerts I., Brys K., De Vreese A., Van Eygen S., Vanfleteren J.R. Axenic growth up-regulates mass-specific metabolic rate, stress resistance, and extends life span in Caenorhabditis elegans. Exp. Gerontol. 2002, 37:1371-1378.
29. Hurwitz I., Fieck A., Read A., Hillesland H., Klein N., Kang A., Durvasula R. Paratransgenic control of vector borne diseases. Int. J. Biol. Sci. 2011, 7:1334-1344.
30. Ikeda T., Yasui C., Hoshino K., Arikawa K., Nishikawa Y. Influence of lactic acid bacteria on longevity of Caenorhabditis elegans and host defense against Salmonella enterica Serovar Enteritidis. Appl. Environ. Microbiol. 2007, 73:6404-6409.
31. Landau I., Boulard Y. Life cycles and morphology. Rodent Malaria 1978, 53-84. Academic Press, London. R. Killick-Kendrick, W. Peters (Eds.).
32. Li M., Wang B., Zhang M., Rantalainen M., Wang S., Zhou H., Zhang Y., Shen J., Pang S., Zhang M., Wei H., Chen Y., Lu H., Zuo J., Su M., Qiu Y., Jia W., Xiao C., Smith L.M., Yang S., Holmes E., Tang H., Zhao G., Nicholson J.K., Li L., Zhao L. Symbiotic gut microbes modulate human metabolic phenotypes. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:2117-2122.
33. MacDonald G. Epidemiology and Control of Malaria 1957, Oxford University Press, London.
34. Maier W.A. Le parasite Plasmodium est-il pathogéne pour le moustique?. Ent. Med. Parasitol. 1980, 189:149-186.
35. Maier W.A., Becker-Feldman H., Seitz H.M. Pathology of malaria-infected mosquitoes. Parasitol. Today 1987, 3:216-218.
36. Mourya D.T., Pidiyar V., Patole M., Gokhale M.D., Shouche V. Effect of midgut bacterial flora of Aedes aegypti on the susceptibility of mosquitoes to dengue viruses. WHO Bull. 2002, 26:190-194.
37. Pumpuni C.B., Beier M.S., Nataro J.P., Guers L.D., Davis J.R. Plasmodium falciparum: inhibition of sporogonic development in Anopheles stephensi by Gram-negative bacteria. Exp. Parasitol. 1993, 77:195-199.
38. Pumpuni C.B., Demaio J., Kent M., Davis J.R., Beier J.C. Bacterial population dynamics in three anopheline species: the impact on Plasmodium sporogonic development. Am. J. Trop. Med. Hyg. 1996, 54:214-218.
39. Ramasamy M.S., Kulasekera R., Wanniarachchi I.C., Srikrishnaraj K.A., Ramasamy R. Interactions of human malaria parasites, Plasmodium vivax and P. falciparum, with the midgut of Anopheles mosquitoes. Med. Vet. Entomol. 1997, 11:290-296.
40. Rani A., Sharma A., Adak T., Bhatnagar R.K. Pseudoxanthomonas icgebensis sp. nov., isolated from the midgut of Anopheles stephensi field-collected larvae. J. Microbiol. 2010, 48:601-606.
41. Rani A., Sharma A., Rajagopal R., Adak T., Bhatnagar R.K. Bacterial diversity analysis of larvae and adult midgut microflora using culture-dependent and culture-independent methods in lab-reared and field-collected Anopheles stephensi - an Asian malarial vector. BMC Microbiol. 2009, 9:96.
42. Ren X., Hoiczyk E., Rasgon J.L. Viral paratransgenesis in the malaria vector Anopheles gambiae. PLoS Pathog. 2008, 4:e1000135.
43. Richards A.G., Brooks M.A. Internal symbiosis in insects. Ann. Rev. Entomol. 1958, 3:37-56.
44. Reisen W.K., Mahmood F. Horizontal life table characteristics of the malaria vectors Anopheles culicifacies and Anopheles stephensi (Diptera: Culicidae). J. Med. Entomol. 1980, 17:211-217.
45. Riehle M.A., Moreira C.K., Lampe D., Lauzon C., Jacobs-Lorena M. Using bacteria to express and display anti- Plasmodium molecules in the mosquito midgut. Int. J. parasitol. 2007, 37:595-603.
46. Rodrigues J., Agrawal N., Sharma A., Malhotra P., Adak T., Chauhan V.S., Bhatnagar R.K. Transcriptional analysis of an immune-responsive serine protease from Indian malarial vector, Anopheles culicifacies. BMC Mol. Biol. 2007, 8:33.
47. Rodrigues J., Brayner F.A., Alves L.C., Dixit R., Barillas-Mury C. Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 2010, 329:1353-1355.
48. Rosengaus R.B., Zecher C.N., Schultheis K.F., Brucker R.M., Bordenstein S.R. Disruption of the termite gut microbiota and its prolonged consequences for fitness. Appl. Environ. Microbiol. 2011, 77:4303-4312.
49. Service M.W. Observations on the ecology of some British mosquitoes. Bull. Entomol. Res. 1967, 59:161-194.
50. Seitz H.M., Maier W.A., Rottok M., Becker-Feldmann H. Concomitant infections of Anopheles stephensi with Plasmodium berghei and Serratia marcescens: additive detrimental effects. Zentralbl. Bakteriol. Mikrobiol. Hyg. A 1987, 266:155-166.
51. Sharma V.P. Current scenario of malaria in India. Parassitologia 1999, 41:349-353.
52. Sharma A., Rodrigues J., Kajla M.K., Agrawal N., Adak T., Bhatnagar R.K. Expression profile of prophenoloxidase-encoding (acppo6) gene of Plasmodium vivax-refractory strain of Anopheles culicifacies. J. Med. Entomol. 2010, 47:1220-1226.
53. Sharma A., Parasher H., Singh O.P., Adak T. Species B of Anopheles culicifacies (Diptera: Culicidae) is reproductively less fit than species A and C of the complex. Acta Trop. 2009, 112:316-319.
54. Straif S.C., Mbogo C.N., Toure A.M., Walker E.D., Kaufman M., Toure Y.T., Beier J.C. Midgut bacteria in Anopheles gambiae and An. funestus (Diptera: Culicidae) from Kenya and Mali. J. Med. Entomol. 1998, 35:222-226.
55. Terashima J., Bownes M. Translating available food into the number of eggs laid by Drosophila. Genetics 2004, 167:1711-1719.
56. Wang S., Ghosh A.K., Bongio N., Stebbings K.A., Lamp D.J., Jacobs-Lorenaa M. Fighting malaria with engineered symbiotic bacteria from vector mosquitoes. Proc. Natl. Acad. Sci. U S A. 2012, 109:12734-12739.
57. Washino R.K., Bailey S.F. Overwintering of Anopheles punctipennis (Diptera: Culicidae) in California. J. Med. Entomol. 1970, 7:95-98.
58. Weiss B., Aksoy S. Microbiome influences on insect host vector competence. Trends Parasitol. 2011, 27:514-522.
59. Zouache K., Raharimalala F.N., Raquin V., Tran-Van V., Raveloson L.H., Ravelonandro P., Mavingui P. Bacterial diversity of field-caught mosquitoes Aedes albopictus and Aedes aegypti, from different geographic regions of Madagascar. FEMS Microbiol. Ecol. 2011, 75:377-389.